Journal of Chemical Ecology

, Volume 42, Issue 3, pp 270–276 | Cite as

The Presence Of Strange Males’ Odor Induces Behavioral Responses And Elevated Levels Of Low Molecular Weight Proteins Excreted In The Urine Of Mature Water Vole Males (Arvicola amphibius L)

  • Galina G. Nazarova
  • Lyudmila P. Proskurniak
  • Ekaterina I. Yuzhik


We hypothesized that low molecular weight urinary proteins play a role in male-male chemical communication in the water vole, Arvicola ampibius L. We studied the effect of placing soiled litter from strange males into the cage of another sexually mature male on the intensity of its digging and scattering, urination on the litter, and alteration in the levels of low molecular weight proteins (15–25 kDa) excreted in the urine before and after 4 days of exposure as determined by chip electrophoresis. The intensity of digging and scattering was positively correlated with levels of testosterone in serum of males exposed to strange male odors (r = 0.56; P < 0.01), as well as with the concentration of low molecular weight proteins in the donor’s urine (r = 0.52, P < 0.05). At the end of the experiment, the level of low molecular weight protein in excreted urine was elevated in the males exposed to the strange male’s litter. These results highlight the importance of quantitative inter-individual variation of low molecular weight urinary proteins in the modulation of the physiology and behavior of conspecifics.


Arvicola amphibius Urine-marking behavior Chemical communication Testosterone Urine Protein 



The authors express their gratitude for the guidance and equipment provided by employees of the Laboratory of Insect Pathology ISEA SB RAS: Victor Glupov, Ekaterina Grizanova, Ivan Dubovsky. Thanks to two anonymous reviewers for comments and contributions that greatly improved this work. The study was performed under the Program of Fundamental Scientific Research in State Academy of Sciences in 2013-2020 (№ VI.51.1.6).


  1. Aars J, Dallas JF, Piertney SB, Marshall F, Gow JL, Telfer S, Lambin X (2006) Widespread gene flow and high genetic variability in populations of water voles Arvicola terrestris in patchy habitats. Mol Ecol 15:1455–1466CrossRefPubMedGoogle Scholar
  2. Beynon RJ, Hurst JL (2003) Multiple roles of major urinary proteins in the house mouse, Mus domesticus. Biochem Soc Trans 31:142–146CrossRefPubMedGoogle Scholar
  3. Beynon RJ, Hurst JL (2004) Urinary proteins and the modulation of chemical scents in mice and rats. Peptides 25:1553–1563CrossRefPubMedGoogle Scholar
  4. Beynon RJ, Veggerby C, Payne CE, Robertson DH, Gaskell SJ, Humphries RE, Hurst JL (2002) Polymorphism in major urinary proteins: molecular heterogeneity in a wild mouse population. J Chem Ecol 28:1429–1446CrossRefPubMedGoogle Scholar
  5. Briand L, Huet J, Perez V, Lenoir G, Nespoulous C, Boucher Y, Trotier D, Pernollet JC (2000) Odorant and pheromone binding by aphrodisin, a hamster aphrodisiac protein. FEBS Lett 476:179–185CrossRefPubMedGoogle Scholar
  6. Bronson FH (1971) Rodent pheromones. Biol Reprod 4:344–357PubMedGoogle Scholar
  7. Cavaggioni A, Mucignat-Caretta C (2000) Major urinary proteins, α2U-globulins and aphrodisin. Biochim Biophys Acta 1482:218–228CrossRefPubMedGoogle Scholar
  8. Chamero P, Marton TF, Logan DW, Flanagan K, Cruz JR, Saghatelian A, Cravatt BF, Stowers L (2007) Identification of protein pheromones that promote aggressive behavior. Nature 450:899–903CrossRefPubMedGoogle Scholar
  9. Evsikov VI, Nazarova GG, Potapov MA (1994) Female odor choice, male social rank, and sex ratio in the water vole. Adv Biosci 93:303–307Google Scholar
  10. Evsikov VI, Nazarova GG, Potapov MA (1997) Genetic-ecological monitoring of a cyclic population of water voles Arvicola terrestris L. in the south of Western Siberia. Russ J Genet 33:963–972Google Scholar
  11. Evsikov VI, Potapov MA, Muzyka VY (1999) Population ecology of water vole (Arvicola terrestris L.) in Western Siberia. II. spacial etological structure of populations. Sibir Ecol Zhurnal 6:69–77Google Scholar
  12. Flower D (1996) The lipocalin protein family: structure and function. Biochem J 318:1–14CrossRefPubMedPubMedCentralGoogle Scholar
  13. Giller K, Huebbe P, Doering F, Pallauf K, Rimbach G (2013) Major urinary protein 5, a scent communication protein, is regulated by dietary restriction and subsequent re-feeding in mice. Proc Biol Sci 280:20130101CrossRefPubMedPubMedCentralGoogle Scholar
  14. Gleason ED, Fuxjager MJ, Oyegbile TO, Marler CA (2009) Testosterone release and social context: when it occurs and why. Front Neuroendocrinol 30:460–469CrossRefPubMedGoogle Scholar
  15. Gomes LAP, Mira APP, Barata EN (2013) The role of scent-marking in patchy and highly fragmented populations of the cabrera vole (Microtus cabrerae Thomas, 1906). Zool Sci 30:248–254CrossRefPubMedGoogle Scholar
  16. Gromov IM, Erbajeva MA (1995) The mammals of Russia and adjacent territories. Lagomorphs and rodents. Zoological Institute, St.- PetersburgGoogle Scholar
  17. Gуmez-Baena G, Armstrong SD, Phelan MM, Hurst JL, Beynon RJ (2014) The major urinary protein system in the rat. Biochem Soc Trans 42:886–892CrossRefGoogle Scholar
  18. Hurst JL, Payne CE, Nevison CM, Marie AD, Humphries RE, Robertson DH, Cavaggioni A, Beynon RJ (2001) Individual recognition in mice mediated by major urinary proteins. Nature 414:631–634CrossRefPubMedGoogle Scholar
  19. Janotova K, Stopka P (2011) The level of major urinary proteins is socially regulated in wild Mus musculus musculus. J Chem Ecol 37:647–656CrossRefPubMedGoogle Scholar
  20. Jeppsson B (1990) Effects of density and resources on the social system of water voles. In: Tamarin RH, Ostfeld RS, Pugh SR, Bujalska G (eds) Social systems and population cycles in voles. Birkhauser Verlag, Basel, pp. 213–226CrossRefGoogle Scholar
  21. Johnston RE (2003) Chemical communication in rodents: from pheromones to individual recognition. J Mammal 84:1141–1162CrossRefGoogle Scholar
  22. Kaur AW, Ackels T, Kuo TH, Cichy A, Dey S, Hays C, Kateri M, Logan DW, Marton TF, Spehr M, Stowers L (2014) Murine pheromone proteins constitute a context-dependent combinatorial code governing multiple social behaviors. Cell 157:676–688CrossRefPubMedPubMedCentralGoogle Scholar
  23. Kudryavtseva NN, Bondar NP, Avgustinovich DF (2004) Effects of repeated experience of aggression on the aggressive motivation and development of anxiety in male mice. Neurosci Behav Physiol 34:721–730CrossRefPubMedGoogle Scholar
  24. Leinders-Zufall T, Brennan PA, Widmayer P, Chandramani P, Chandramani PS, Maul-Pavicic A, Jager M, Li X-H, Breer H, Zufall F, Boehm T (2004) MHC class I peptides as chemosensory signals in the vomeronasal organ. Science 306:1033–1037CrossRefPubMedGoogle Scholar
  25. Logan DW, Marton TF, Stowers L (2008) Species specificity in major urinary proteins by parallel evolution. PLoS One 3:e3280CrossRefPubMedPubMedCentralGoogle Scholar
  26. Marchlewska-Koj A, Cavaggioni A, Mucignat-Caretta C, Olejniczak PL (2000) Stimulation of estrus in female mice by male urinary proteins. J Chem Ecol 26:2355–2366CrossRefGoogle Scholar
  27. Moorhouse TP, Macdonald DW (2008) What limits male range sizes at different population densities? evidence from three populations of water voles. J Zool 274:395–402CrossRefGoogle Scholar
  28. More L (2006) Mouse major urinary proteins trigger ovulation via the vomeronasal organ. Chem Senses 31:393–401CrossRefPubMedGoogle Scholar
  29. Mucignat-Caretta C, Caretta A, Cavaggioni A (1995) Acceleration of puberty onset in female mice by male urinary proteins. J Physiol 486:517–522CrossRefPubMedPubMedCentralGoogle Scholar
  30. Naumov NP (1975) Biological (signal) fields and their importance in the life of mammals. West USSR Academy Of Sciences 2:55–62Google Scholar
  31. Nazarova GG (2011) Anogenital distance as a prognostic characteristic of sexual maturity in water voles (Arvicola terrestris). Zoologičeskij žurnal 90:121–122Google Scholar
  32. Nazarova GG, Proskurnyak LP (2013) Protein content in urine of male and female water vole (Arvicola amphibius) at the period of spring growth and sexual maturation. J Evol Biochem Physiol 49:360–364CrossRefGoogle Scholar
  33. Nelson AC, Cauceglia JW, Merkley SD, Youngson NA, Oler AJ, Nelson RJ, Cairns BR, Whitelaw E, Potts WK (2013) Reintroducing domesticated wild mice to sociality induces adaptive transgenerational effects on MUP expression. Proc Natl Acad Sci U S A 110:19848–19853CrossRefPubMedPubMedCentralGoogle Scholar
  34. Novikov SN, Churakov GA, Filimonenko AA, Ermakova II, Fedorova EM, Burkot IA (2009) The pattern of major urinary proteins (MUPS) expression during postnatal ontogenesis of a laboratory mouse depends on genotype and sex. Ontogenez 40:261–269PubMedGoogle Scholar
  35. Novotny M, Harvey S, Jemiolo B, Alberts J (1985) Synthetic pheromones that promote inter-male aggression in mice. Proc Natl Acad Sci U S A 82:2059–2061CrossRefPubMedPubMedCentralGoogle Scholar
  36. Novotny M, Harvey S, Jemiolo B (1990) Chemistry of male dominance in the house mouse, Mus domesticus. Experientia 46:109–113CrossRefPubMedGoogle Scholar
  37. Overath P, Sturm T, Rammensee HG (2014) Of volatiles and peptides: In search for MHC-dependent olfactory signals in social communication. Cell Mol Life Sci 13:2429–2442CrossRefGoogle Scholar
  38. Panteleev PA (1971) Population ecology of the water vole. In: DM S (ed) National Lending Library for Science and Technology, Translated edn. Massachusetts, Boston, p. 358 ppGoogle Scholar
  39. Plusnin YM, Evsikov VI (1985) Seasonal differences in social structure of demes in the water vole (Arvicola terrestris). Ekoloji 3:47–55Google Scholar
  40. Potapov MA, Rogov VG, Ovchinnikova LE, Muzyka VY, Potapova OF, Bragin AV, Evsikov VI (2004) The effect of winter food stores on body mass and winter survival of water voles, Arvicola terrestris, in Western Siberia: the implications for population dynamics. Folia Zool 53:37–46Google Scholar
  41. Robertson DHL, Beynon RJ, Evershed RP (1993) Extraction, characterization, and binding analysis of two pheromonally active ligands associated with majory urinary protein of house mouse (Mus musculus). J Chem Ecol 19:1405–1416CrossRefPubMedGoogle Scholar
  42. Ruff JS, Nelson AC, Kubinak JL, Potts WK (2012) MHC signaling during social communication. Adv Exp Med Biol 738:290–313CrossRefPubMedPubMedCentralGoogle Scholar
  43. Singer AG, Macrides F, Clancy AN, Agosta WC (1986) Purification and analysis of a proteinaceous aphrodisiac pheromone from hamster vaginal discharge. J Biol Chem 261:13323–12226PubMedGoogle Scholar
  44. Soini HA, Wiesler D, Apfelbach R, König P, Vasilieva NY, Novotny MV (2005) Comparative investigation of the volatile urinary profiles in different phodopus hamster species. J Chem Ecol 31:1125–1143CrossRefPubMedGoogle Scholar
  45. Stoddart DM (1970) Individual range, dispersion and dispersal in a population of water voles (Arvicola terrestris [L.]). J Anim Ecol 39:403–425CrossRefGoogle Scholar
  46. Stoddart DM (1972) The lateral scent organs of Arvicola terrestris (rodentia:microtinae). J Zool (Lond) 166:49–54CrossRefGoogle Scholar
  47. Stopka P, Janotova K, Heyrovsky D (2007) The advertisement role of major urinary proteins in mice. Physiol Behav 91:667–670CrossRefPubMedGoogle Scholar
  48. Stopková R, Zdrahal Z, Ryba Š, Šedo O, Šandera M, Stopka P (2010) Novel OBP genes similar to hamster aphrodisin in the bank vole, Myodes glareolus. BMC Genomics 11:45CrossRefPubMedPubMedCentralGoogle Scholar
  49. Stopková R, Dudková B, Hájková P, Stopka P (2014) Complementary roles of mouse lipocalins in chemical communication and immunity. Biochem Soc Trans 42:893–898CrossRefPubMedGoogle Scholar
  50. Woodroffe GL, Lawton JH, Davidson WL (1990) Patterns in the production of latrines by water voles (Arvicola terrestris) and their use as indices of abundance in population surveys. J Zool 220:439–445CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  • Galina G. Nazarova
    • 1
  • Lyudmila P. Proskurniak
    • 1
  • Ekaterina I. Yuzhik
    • 1
    • 2
  1. 1.Institute of Systematics and Ecology of AnimalsSiberian Branch RASNovosibirskRussia
  2. 2.Institute of Molecular Pathology and PathomorphologyNovosibirskRussia

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